Degeneration and proliferation of astrocytes in the mouse dentate gyrus after pilocarpine-induced status epilepticus

Experimental Neurology

Volumn 201, Issue 2, 2006, Pages 416-427

  Borges, Karin ^a,c   McDermott, Dayna ^a   Irier, Hasan ^a   Smith, Yoland ^a,b   Dingledine, Raymond ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Adult progenitor cell; Glial fibrillary acidic protein; Hilus; Kainate; Mouse strain; Seizure; Stem cell

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; KAINIC ACID; PILOCARPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; ELECTRON MICROSCOPY; EPILEPSY; EPILEPTIC STATE; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; SEIZURE;

ANIMALS; ASTROCYTES; CELL COUNT; CELL PROLIFERATION; DENTATE GYRUS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED STRAINS; MICROGLIA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NEURONS; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; SPECIES SPECIFICITY; STATUS EPILEPTICUS; TIME FACTORS;

EID: 33748436657     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.04.031     Document Type: Article

References (59)

1. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., and Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10432-10437
2. Bondolfi L., Ermini F., Long J.M., Ingram D.K., and Jucker M. Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol. Aging 25 (2004) 333-340
3. Bordey A., and Spencer D.D. Distinct electrophysiological alterations in dentate gyrus versus CA1 glial cells from epileptic humans with temporal lobe sclerosis. Epilepsy Res. 59 (2004) 107-122
4. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., and Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol. 182 (2003) 21-34
5. Borges K., Irier H., McDermott D., Hubert W., Smith Y., and Dingledine R. Region-specific astrocyte degeneration after pilocarpine-induced status epilepticus. Abstr. Soc. Neurosci. 33rd Ann. Meeting, No. 378.16 (2003)
6. Borges K., McDermott D.L., and Dingledine R. Reciprocal changes of CD44 and GAP-43 expression in the dentate gyrus inner molecular layer after status epilepticus in mice. Exp. Neurol. 188 (2004) 1-10
7. Bushong E.A., Martone M.E., Jones Y.Z., and Ellisman M.H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22 (2002) 183-192
8. Clifford D.B., Olney J.W., Maniotis A., Collins R.C., and Zorumski C.F. The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience 23 (1987) 953-968
9. Eckenhoff M.F., and Rakic P. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J. Neurosci. 8 (1988) 2729-2747
10. Eid T., Thomas M.J., Spencer D.D., Runden-Pran E., Lai J.C., Malthankar G.V., Kim J.H., Danbolt N.C., Ottersen O.P., and de Lanerolle N.C. Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 363 (2004) 28-37
11. Eng L.F., Yu A.C., and Lee Y.L. Astrocytic response to injury. Prog. Brain Res. 94 (1992) 353-365
12. Ferland R.J., Gross R.A., and Applegate C.D. Increased mitotic activity in the dentate gyrus of the hippocampus of adult C57BL/6J mice exposed to the flurothyl kindling model of epileptogenesis. Neuroscience 115 (2002) 669-683
13. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L.P., Yamaguchi M., Kettenmann H., and Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23 (2003) 373-382
14. Gabriel S., Njunting M., Pomper J.K., Merschhemke M., Sanabria E.R., Eilers A., Kivi A., Zeller M., Meencke H.J., Cavalheiro E.A., Heinemann U., and Lehmann T.N. Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis. J. Neurosci. 24 (2004) 10416-10430
15. Gage F.H., Kempermann G., Palmer T.D., Peterson D.A., and Ray J. Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36 (1998) 249-266
16. Garcia A.D., Doan N.B., Imura T., Bush T.G., and Sofroniew M.V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7 (2004) 1233-1241
17. Gouder N., Scheurer L., Fritschy J.M., and Boison D. Overexpression of adenosine kinase in epileptic hippocampus contributes to epileptogenesis. J. Neurosci. 24 (2004) 692-701
18. Gurnett C.A., Landt M., and Wong M. Analysis of cerebrospinal fluid glial fibrillary acidic protein after seizures in children. Epilepsia 44 (2003) 1455-1458
19. Hinterkeuser S., Schroder W., Hager G., Seifert G., Blumcke I., Elger C.E., Schramm J., and Steinhauser C. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur. J. Neurosci. 12 (2000) 2087-2096
20. Hof P., Young W.G., Bloom F.E., Belichenko P.V., and Celio M.R. Comparative Cytoarchitonic Atlas of the C57BL/6 and 129/Sv Mouse Brains (2000), Elsevier, New York
21. Huttmann K., Sadgrove M., Wallraff A., Hinterkeuser S., Kirchhoff F., Steinhauser C., and Gray W.P. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur. J. Neurosci. 18 (2003) 2769-2778
22. Jorgensen M.B., Finsen B.R., Jensen M.B., Castellano B., Diemer N.H., and Zimmer J. Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp. Neurol. 120 (1993) 70-88
23. Kempermann G., and Gage F.H. Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res. Dev. Brain Res. 134 (2002) 1-12
24. Kempermann G., Jessberger S., Steiner B., and Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27 (2004) 447-452
25. Kettenmann H., and Ransom B.R. Neuroglia. 2nd ed. (2004), Oxford University Press, Oxford, UK
26. Kligman D., and Hilt D.C. The S100 protein family. Trends Biochem. Sci. 13 (1988) 437-443
27. Krum J.M. Experimental gliopathy in the adult rat CNS: effect on the blood-spinal cord barrier. Glia 11 (1994) 354-366
28. Lahteinen S., Pitkanen A., Saarelainen T., Nissinen J., Koponen E., and Castren E. Decreased BDNF signalling in transgenic mice reduces epileptogenesis. Eur. J. Neurosci. 15 (2002) 721-734
29. Liaw L., Birk D.E., Ballas C.B., Whitsitt J.S., Davidson J.M., and Hogan B.L. Altered wound healing in mice lacking a functional osteopontin gene (spp1). J. Clin. Invest. 101 (1998) 1468-1478
30. Lie D.C., Song H., Colamarino S.A., Ming G.L., and Gage F.H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 399-421
31. Motte J., Fernandes M.J., Baram T.Z., and Nehlig A. Spatial and temporal evolution of neuronal activation, stress and injury in lithium-pilocarpine seizures in adult rats. Brain Res. 793 (1998) 61-72
32. Nadler J.V. The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res. 28 (2003) 1649-1658
33. Nadler J.V., Perry B.W., Gentry C., and Cotman C.W. Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J. Comp. Neurol. 192 (1980) 333-359
34. Newman E.A. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26 (2003) 536-542
35. Niquet J., Ben-Ari Y., and Represa A. Glial reaction after seizure induced hippocampal lesion: immunohistochemical characterization of proliferating glial cells. J. Neurocytol. 23 (1994) 641-656
36. Nitecka L., Tremblay E., Charton G., Bouillot J.P., Berger M.L., and Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat: II. Histopathological sequelae. Neuroscience 13 (1984) 1073-1094
37. Ogata K., and Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113 (2002) 221-233
38. Ohm T.G., Jung E., and Schnecko A. A subpopulation of hippocampal glial cells specific for the zinc-containing mossy fibre zone in man. Neurosci. Lett. 145 (1992) 181-184
39. Palmer T.D., Willhoite A.R., and Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425 (2000) 479-494
40. Parent J.M. Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 9 (2003) 261-272
41. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
42. Paulsen R.E., Contestabile A., Villani L., and Fonnum F. An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J. Neurochem. 48 (1987) 1377-1385
43. Peters A., Palay S.L., and Webster H. The Fine Structure of the Nervous System: Neurons and their Supporting Cells. 3rd ed. (1991), Oxford University Press, Oxford 494 pp.
44. Petito C.K., Olarte J.P., Roberts B., Nowak Jr. T.S., and Pulsinelli W.A. Selective glial vulnerability following transient global ischemia in rat brain. J. Neuropathol. Exp. Neurol. 57 (1998) 231-238
45. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 19 (2004) 234-246
46. Revuelta M., Castano A., Machado A., Cano J., and Venero J.L. Kainate-induced zinc translocation from presynaptic terminals causes neuronal and astroglial cell death and mRNA loss of BDNF receptors in the hippocampal formation and amygdala. J. Neurosci. Res. 82 (2005) 184-195
47. Rittling S.R., Matsumoto H.N., McKee M.D., Nanci A., An X.R., Novick K.E., Kowalski A.J., Noda M., and Denhardt D.T. Mice lacking osteopontin show normal development and bone structure but display altered osteoclast formation in vitro. J. Bone Miner. Res. 13 (1998) 1101-1111
48. Schauwecker P.E., and Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 4103-4108
49. Schipper H.M. Gomori-positive astrocytes: biological properties and implications for neurologic and neuroendocrine disorders. Glia 4 (1991) 365-377
50. Schipper H.M. Astrocytes, brain aging, and neurodegeneration. Neurobiol. Aging 17 (1996) 467-480
51. Scott B.W., Wojtowicz J.M., and Burnham W.M. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp. Neurol. 165 (2000) 231-236
52. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
53. Seri B., Garcia-Verdugo J.M., Collado-Morente L., McEwen B.S., and Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 478 (2004) 359-378
54. Sharp F.R., Liu J., and Bernabeu R. Neurogenesis following brain ischemia. Brain Res. Dev. Brain Res. 134 (2002) 23-30
55. Steiner B., Kronenberg G., Jessberger S., Brandt M.D., Reuter K., and Kempermann G. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46 (2004) 41-52
56. Thomas L.B., Gates D.J., Richfield E.K., O'Brien T.F., Schweitzer J.B., and Steindler D.A. DNA end labeling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp. Neurol. 133 (1995) 265-272
57. Tian G.F., Azmi H., Takano T., Xu Q., Peng W., Lin J., Oberheim N., Lou N., Wang X., Zielke H.R., Kang J., and Nedergaard M. An astrocytic basis of epilepsy. Nat. Med. 11 (2005) 973-981
58. Willis C.L., Nolan C.C., Reith S.N., Lister T., Prior M.J., Guerin C.J., Mavroudis G., and Ray D.E. Focal astrocyte loss is followed by microvascular damage, with subsequent repair of the blood-brain barrier in the apparent absence of direct astrocytic contact. Glia 45 (2004) 325-337
59. Willoughby J.O., Mackenzie L., Broberg M., Thoren A.E., Medvedev A., Sims N.R., and Nilsson M. Fluorocitrate-mediated astroglial dysfunction causes seizures. J. Neurosci. Res. 74 (2003) 160-166